Speech encoding by coupled cortical theta and gamma oscillations.

Alexandre Hyafil,Boris Gutkin,Lorenzo Fontolan,Anne-Lise Giraud,Claire Kabdebon

doi:10.7554/elife.06213

Abstract

Many environmental stimuli present a quasi-rhythmic structure at different timescales that the brain needs to decompose and integrate. Cortical oscillations have been proposed as instruments of sensory de-multiplexing, i.e., the parallel processing of different frequency streams in sensory signals. Yet their causal role in such a process has never been demonstrated. Here, we used a neural microcircuit model to address whether coupled theta-gamma oscillations, as observed in human auditory cortex, could underpin the multiscale sensory analysis of speech. We show that, in continuous speech, theta oscillations can flexibly track the syllabic rhythm and temporally organize the phoneme-level response of gamma neurons into a code that enables syllable identification. The tracking of slow speech fluctuations by theta oscillations, and its coupling to gamma-spiking activity both appeared as critical features for accurate speech encoding. These results demonstrate that cortical oscillations can be a key instrument of speech de-multiplexing, parsing, and encoding.

Highlights

The physical complexity of biological and environmental signals poses a fundamental problem to the sensory systems
Direct evidence for a local generation of theta oscillations in auditory cortex is still scarce (Ainsworth et al, 2011) and we cannot completely rule out that they might spread from remote generators
We built the case for local generation from the following facts: (1) neocortical theta oscillations are observed in vitro (Fanselow et al, 2008), (2) MEG, EEG, and combined EEG/FMRI recordings in humans show that theta activity phase-locks to speech amplitude envelope in A1 and immediate association cortex—but not beyond—(Ahissar et al, 2001; Luo and Poeppel, 2007; Cogan and Poeppel, 2011; Morillon et al, 2012), and (3) theta phase-locking to speech is not accompanied by power increase, arguing for a phase restructuring of a local oscillation (Luo and Poeppel, 2007)

Summary

Introduction

The physical complexity of biological and environmental signals poses a fundamental problem to the sensory systems. The control of gamma by theta oscillations could both modulate the excitability of gamma neurons to devote more processing power to the informative parts of syllabic sound patterns, and constitute a reference time frame aligned on syllabic contours for interpreting gamma-based phonemic processing (Shamir et al, 2009; Ghitza, 2011; Kayser et al, 2012; Panzeri et al, 2014). Compelling as this hypothesis may sound, direct evidence for neural mechanisms linking speech constituents and oscillatory components is still lacking.

Results

Discussion

Materials and methods